Do food availability parasitism and stress have synergistic effects on red colobus
populations living in forest fragments.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 131:525–534 (2006)
Do Food Availability, Parasitism, and Stress Have
Synergistic Effects on Red Colobus Populations
Living in Forest Fragments?
Colin A. Chapman,1,2* Michael D. Wasserman,3 Thomas R. Gillespie,4,5 Michaela L. Speirs,1
Michael J. Lawes,6 Tania L. Saj,7 and Toni E. Ziegler8
1
Department of Anthropology and McGill School of Environment, McGill University, Montreal, QC H3A 2T7, Canada
Wildlife Conservation Society, Bronx, NY 10460
3
Department of Environmental Science, Policy, and Management, University of California, Berkeley, CA 94720
4
Department of Anthropology, University of Illinois, Urbana, IL 61802
5
Department of Veterinary Pathobiology, University of Illinois, Urbana, IL 61802
6
School of Biological and Conservation Sciences, Forest Biodiversity Research Unit, University of KwaZulu-Natal,
Scottsville 3209, South Africa
7
Department of Anthropology, McGill University, Montreal, QC H3A 2T7, Canada
8
National Primate Research Center and Department of Psychology, University of Wisconsin, Madison, WI 53715
2
KEY WORDS
colobus
population regulation; primate conservation; parasitism; fragmentation; cortisol;
ABSTRACT
Identifying factors that inﬂuence animal
density is a fundamental goal in ecology that has taken
on new importance with the need to develop informed
management plans. This is particularly the case for primates as the tropical forest that supports many species
is being rapidly converted. We use a system of forest
fragments adjacent to Kibale National Park, Uganda, to
examine if food availability and parasite infections have
synergistic affects on red colobus (Piliocolobus tephrosceles) abundance. Given that the size of primate populations can often respond slowly to environmental changes,
we also examined how these factors inﬂuenced cortisol
levels. To meet these objectives, we monitored gastrointestinal parasites, evaluated fecal cortisol levels, and
determined changes in food availability by conducting
complete tree inventories in eight fragments in 2000 and
2003. Red colobus populations declined by an average of
21% among the fragments; however, population change
ranged from a 25% increase to a 57% decline. The cumulative basal area of food trees declined by an average of
29.5%; however, forest change was highly variable (a 2%
gain to a 71% decline). We found that nematode prevalence averaged 58% among fragments (range 29–83%).
The change in colobus population size was correlated
both with food availability and a number of indices of
parasite infections. A path analysis suggests that change
in food availability has a strong direct effect on population size, but it also has an indirect effect via parasite infections. Am J Phys Anthropol 131:525–534,
2006. V 2006 Wiley-Liss, Inc.
A fundamental goal in ecology is identifying factors
determining animal population abundance (Boutin,
1990). The importance of this goal has increased with
the need to develop informed management plans for
endangered or threatened species. With respect to folivores, building on the pioneering work of Milton (1979),
several researchers have indicated the importance of
protein availability in determining folivore abundance,
and several subsequent studies have found positive correlations between colobine biomass and the ratio of protein to ﬁber, both at local (Chapman and Chapman,
2002; Chapman et al., 2002a, 2004a; Ganzhorn, 2002)
and regional scales (Oates et al., 1990; Davies, 1994).
While this information will be useful in conservation
planning, ﬁnding single factor explanations for complex
biological phenomena, such as determinants of folivore
abundance, is unlikely. Rather, long-term studies have
highlighted the importance of multifactoral explanations.
For example, based on a 68-month study of the effect of
the parasitic bot ﬂy (Alouattamyia baeri) on howler monkeys (Alouatta palliata), Milton (1996) concluded that
the annual pattern of howler mortality results from a
combination of effects, including age, physical condition,
and larval burden of the parasitized individual, which
becomes critical when the population experiences dietary
stress. Similarly, Gulland (1992) studied the interactions
of Soay sheep and nematode parasites and demonstrated
that at times of population crashes sheep were emaciated, had high nematode burdens, and showed signs of
protein-energy malnutrition. In the ﬁeld, sheep treated
with antihelminthics had lower mortality rates, while
C 2006
V
WILEY-LISS, INC.
C
Grant sponsors: Canadian Research Chairs Program; Wildlife
Conservation Society; Natural Science and Engineering Research
Council of Canada; National Science Foundation.
*Correspondence to: Colin A. Chapman, Department of Anthropology and McGill School of Environment, 855 Sherbrooke Street West,
McGill University, Montreal H3A 2T7, Canada.
E-mail: colin.chapman@mcgill.ca
Received 13 December 2005; accepted 12 May 2006
DOI 10.1002/ajpa.20477
Published online 6 September 2006 in Wiley InterScience
(www.interscience.wiley.com).
526
C.A. CHAPMAN ET AL.
experimentally infected sheep with high parasite loads,
but fed nutritious diets, showed no sign of malnutrition.
It is possible that disease/parasitism and nutrition often
interact to determine the abundance of wildlife populations. Helminthic and protozoal parasites can impact host
survival and reproduction directly through pathological
effects and indirectly by reducing host condition (Coop
and Holmes, 1996; Murray et al., 1998). Severe parasitosis
can lead to blood loss, tissue damage, spontaneous abortion, congenital malformations, and death (Collias and
Southwick, 1952; Despommier et al., 1995). However, less
severe infections are more common and they may compromise digestion or nutrient absorption, increase energy expenditure, and impair travel, feeding, predator escape,
and competition for resources or mates (Hudson et al.,
1992; Coop and Holmes, 1996). Some parasites extract signiﬁcant amounts of nutrients from hosts, resulting in
marked reduction in energy uptake (Moller et al., 1994),
but others appear to cause little or no effect on host energetics (Munger and Karasov, 1989). Animal body condition
and reproductive status can be compromised when parasites inﬂict substantial energetic costs (Hudson, 1986;
Toque, 1993). However, parasites do not necessarily induce
negative effects if hosts have adequate energy reserves or
nutrient supplies concurrent with infection (Munger and
Karasov, 1989; Gulland, 1992; Milton, 1996), suggesting
that the outcome of host–parasite associations may be contingent on host nutritional status, as well as on the severity of infection.
Dietary stress may exacerbate the clinical consequences of parasitic infection through immunosuppression
(Holmes, 1995; Milton, 1996). If so, then food shortages
could result in higher parasite burden, which in turn
could increase nutritional demands on the host and exacerbate the effects of food shortages. If this occurred,
nutritional status and parasitism would have synergistic
effects on the host, i.e., the individual effects of each factor would be ampliﬁed when co-occurring. The interactions between nutritional stress and parasitism have
been examined in a number of laboratory studies (Keymer and Hiorns, 1986; Munger and Karasov, 1989) and a
handful of ﬁeld studies (Gulland, 1992; Toque, 1993;
Murray et al., 1998), and they have led to speculation
that vertebrate populations may be inﬂuenced by interactive effects of food shortage and parasitism (Keymer
and Hiorns, 1986; Holmes, 1995; Murray et al., 1998).
One limitation of many previous studies exploring the
potential for a synergism between nutritional status and
parasite infections in wild populations is that researchers must monitor populations over considerable periods
of time to repeatedly witness if changes in nutritional
status and parasite infections are associated with
changes in host population size. Here we attempt to circumvent this limitation in two ways. First, we examine
a series of populations where food availability was
thought to differ markedly (Onderdonk and Chapman,
2000; Chapman et al., 2004a). Anthropogenic fragmentation often produces isolated populations where food
availability differs among fragments (Laurance and Bierregaard, 1997) and potentially harboring different parasite infections. This makes it possible to obtain the sample size of what can be considered independent populations to correlate population change to food availability
and level of parasite infection.
Second, we explore the use of stress hormones to monitor
the status of populations. Research on captive mammals
and humans demonstrates that high and prolonged ele-
vated glucocorticoid levels (cortisol is one type of glucocorticoid) typically reduces survival and reproduction (Wasser
et al., 1997; Creel, 2001; Creel et al., 2002; Bercovitch and
Ziegler, 2002). Although data on ﬁtness effects of elevated
glucocorticoid levels in the wild are currently limited, the
expectation from lab studies is that ﬁtness will decrease as
population level stressors become more severe or more prolonged (Boonstra and Singleton, 1993; Creel et al., 2002).
Here we examine if a population’s average cortisol level is
correlated with the food available to the population or its
parasite infections. If positive associations are found, it is
reasonable to assume that populations with high cortisol
levels are physiologically challenged, and in the long run,
they will suffer reduced survival and reproduction. As well
as considering a population’s average cortisol level, we evaluate the degree of variation in cortisol levels. Here we
assume that high variance in cortisol levels indicate that
some individuals in the population are more stressed than
others. With social primates, it is most likely that variation
in cortisol levels will be a function of dominance, but
unfortunately, it is not clear how cortisol will vary in association with dominance. Dominant individuals may have
improved access to resources that could boost overall condition and immunocompetence (Abbott et al., 2003). Alternatively, increased levels of aggression associated with high
rank may lead to higher levels of testosterone and stress,
which could lead to greater susceptibility to parasite infections (Combes, 2001). Potentially reﬂecting these alternative possibilities, conﬂicting or ambiguous empirical patterns have been found to date between dominance and parasite infection levels in primates. For example, Hausfater
and Watson (1976) documented that dominant yellow
baboons (Papio cynocephalus) had higher outputs of helminth eggs. In contrast, Muller-Graf et al. (1996) found no
association between dominance rank and indices of helminth infection in olive baboons (P. anubis), while Eley
et al. (1989) have documented that lice were more common
on low-ranking olive baboons.
Since 1995 we have been studying the colobus populations inhabiting a series of forest fragments outside of
Kibale National Park, Uganda. These fragments are
community owned, and each has experienced a different
history of land use. This setting, along with knowledge
of the population dynamics of the colobus in each fragment, offers a quasi-experimental setting, with each
fragment being an independent population, since dispersal among fragments is rare. Therefore, it is possible to
relate patterns of population change to food availability
and disease proﬁles of these populations.
The purpose of this research was to use this setting to
examine if food availability and parasite infections could
have synergistic affects on red colobus (Piliocolobus tephrosceles) and inﬂuence their abundance. Given that primate population size can respond very slowly to even
dramatic environmental change (Struhsaker, 1976), we
wanted to evaluate how food availability and parasite
infections inﬂuenced a more immediate measure of
stress. Thus, we determined if food availability and parasite infections predicted the populations’ fecal cortisol
levels, and whether there were any indications that this
index of stress was related to population change.
METHODS
Sites and samples
Since 1995 we have studied 19 forest fragments neighboring Kibale National Park (795 km2) in western
American Journal of Physical Anthropology—DOI 10.1002/ajpa
FOOD AVAILABILITY, PARASITISM, AND STRESS
Uganda (Onderdonk and Chapman, 2000; Chapman
et al., 2004a). As part of this program, we determined
the population size of red colobus in 11 remaining fragments in May through November 2000 and again from
May through July 2003. Unfortunately, some of these
populations are currently very small, thus for analyses
of population change we consider those eight fragments
censused in 2000 and 2003 that had a reasonably sized
red colobus populations in 2000 (average 17 individuals,
range 7–24).
Kibale is a mid-altitude, moist-evergreen forest receiving 1712 mm of rainfall annually (1990–2004) during
two rainy seasons (Chapman et al., 2004b). Prior to
clearing for agriculture, there was likely continuous forest throughout the region. Now only small pockets of forest remain in areas unsuitable for agriculture. These
fragments are community owned, thus they are
degraded to varying degrees depending on the needs of
the neighboring households (Naughton-Treves and Chapman, 2002). Around Kibale, people use land primarily
for smallholder farming (54% of the area within 1 km)
and human population density is *272 individuals/km2.
Farms near Kibale average 1.4 hectare, of which on average 40% lies fallow (Naughton-Treves, 1998).
Forest fragments were originally selected if they had a
clearly deﬁned boundary, were isolated from other fragments or tracts of forest by 50 m, and were small
enough to count all primate groups (Onderdonk and
Chapman, 2000). To obtain reliable estimates of population size, observers often stayed with a group for up to
12 h and wait for members to make a coordinated movement across an opening in the canopy. Given our sampling effort and small fragment size, we believe that we
obtained a complete census of all individuals. Even
though fragments could be fairly close to one another,
red colobus appeared to be very hesitant to move on the
ground among fragments. During monthly sampling of
one fragment over the last 13 years (Chapman et al.,
1998) and over 330 h of behavioral observation, we never
observed a group make a temporary visit to this fragment; however, a permanent move was seen when a distant fragment was largely deforested (Chapman et al.,
2005).
Assessment of parasite community
From August 1999 to June 2004, we collected 634 fecal
samples from red colobus in forest fragments (mean per
fragment 79.4). Fecal samples were collected, stored
individually in 10% formalin solution, and processed
using concentration by sodium nitrate ﬂotation and fecal
sedimentation (Sloss et al., 1994). Eggs and larvae of
parasites were counted and identiﬁed on the basis of egg
color, shape, contents, and size. Coprocultures and necropsies were used to match parasite eggs to larvae for
positive identiﬁcation (Gillespie et al., 2005a,b).
The parasite infections were described in terms of
prevalence of infection, richness, and multiple infections.
Comparisons of parasite prevalence can be a useful indicator that parasites may be impacting host populations
(i.e., population declines have been correlated to increased
infection prevalence). Prevalence is the proportion of individuals sampled that are infected with a particular parasite. Since we could not individually recognize each animal
in the population each year, we attempted to collect samples in a short period of time once each year and we tried
to rotate among individuals so as not to repeatedly sample
527
the same individual. However, repeat samples likely
occurred and thus this should be viewed as an index of
prevalence. This is a concern since a small number of animals with consistently high infection levels and high richness could be over-represented in the sampling scheme,
particularly since sick animals can defecate more than
healthy individuals (see Muehlenbein, 2005 for a discussion of this issue). In a quantitative evaluation of this
issue Huffman et al. (1997) contrasted incidences of infection based on the number of fecal samples obtained from
chimpanzees (Pan troglodytes) from Mahale, Tanzania versus that based on the number of known individuals and
documented that individual infection rates, the preferred
unit of comparison, were statistically higher than rates
based on all samples. The frequency of multiple-species
infections (i.e., the proportion of a population with >1 species of parasite) can be another useful index, as multiplespecies infections are associated with a greater potential
for morbidity and mortality. Richness is the number of
unique intestinal species documented from the host’s fecal
sample and an increase in richness could be indicative of
greater morbidity. Parasite egg production is often highly
variable and thus may not be indicative of actual infection
intensity; however, it is frequently reported to describe
infections (e.g., Gulland, 1992; Ezenwa, 2003). With Trichuris sp. from red colobus we typically obtain <10 eggs/g;
however, for some groups at some times animals consistently have over 300 egg/g (all individuals in a group for
an extended time). This suggests that this might be a useful index of parasite infection, but we suggest that the
results be viewed critically and only be considered of interest if they are in concordance with other indices of parasite infection.
Assessment of stress––Cortisol
To evaluate fecal cortisol, 98 fecal samples (average
12.3 per fragment, range 8–24) were collected in 2003
(primarily June) from the eight fragments, and the age
and sex of the animal was determined. As fecal steroid
levels can vary along a number of dimensions, the conditions under which samples were collected were carefully
deﬁned. First, all samples were collected between 0800
and 1400 hrs to reduce variation that can be caused by
diel variation in the excretion patterns of fecal steroids
(Sousa and Ziegler, 1998). However, this is still a fairly
long diurnal period, thus to examine diurnal variation in
more detail, fecal samples were collected from four adult
males and four adult females with infant, with each individual followed for one day (0800–1800 hrs), for a total
of eight days of sampling within Kibale National Park.
We documented that fecal cortisol levels did vary over
the course of the day (1.9% increase per h) and that this
pattern of variation was the same for all individuals
(Wasserman and Chapman, unpublished data). If we
compare levels from the earliest to the latest hour that
samples were collected, there would be an 11.6% increase. Thus, in the analysis presented, the cortisol samples were adjusted to the most common time that samples were selected, even though there was no signiﬁcant
difference between fragments in the time of collection (F
¼ 0.1422, P ¼ 0.207).
Second, since cortisol levels increase with maturation
(Bercovitch and Clarke, 1995), samples were collected
only from adult animals. Third, because cortisol changes
in association with pregnancy and it is not possible to
determine when a female is in the early stages of preg-
American Journal of Physical Anthropology—DOI 10.1002/ajpa
528
C.A. CHAPMAN ET AL.
nancy, samples were only collected from adult males and
females with young infants. Finally, the lag time
between a stress event (i.e., the appearance of steroids
in the plasma) and appearance of steroids in the feces
varies among species, but is typically between 12 h and
2 days (Schwarzenberger et al., 1996). Since the presence of observers may stress animals, samples were collected on the ﬁrst day of observation, and then, at least
a 7-day break was taken before any additional samples
were taken.
We attempted to collect a single sample from all adult
males and females with infant in each group that met
our selection criteria (i.e., the group was large enough)
in each of the eight fragments. This was done each day
we visited a fragment, with collections typically made on
2–3 different days for each group. Upon defecation, samples were immediately placed in vials stored on ice. At
the end of the day the samples were transferred to a
208C freezer and stored until lab analyses. Fecal cortisol and metabolites were solubilized from a 0.5-g sample
of fecal material using a 5.0 pH citrate buffer and 95%
ethanol solution that was mixed for 21–27 h. After extraction, samples were place in a centrifuge for 30 min.
This supernatant (with solubilized hormones) was processed by passing 2 ml of supernatant through an Alltech maxi-clean ﬁlter cartridge. These cartridges were
analyzed at the National Primate Research Center at
the University of Wisconsin-Madison. The cartridges
were washed with 1 ml of 20% methanol and the columns were eluted with 2 ml methanol. This methanol
was dried, resuspended in 1 ml ethanol, and 50 ll was
taken for the EIA (enzymeimmunoassay). The assay followed the methods reported in Ziegler et al. (1995).
These analyses provided data on the metabolites of cortisol found in the supernatant, validated the EIA, and
resulted in a measure of the amount of cortisol and
metabolites in each sample in nanogram per gram of dry
feces. The dry weight of each sample was calculated in
the ﬁeld by drying to constant weight and calculating
the percent water. Parallelism was demonstrated using
serial dilution curves, with no signiﬁcant difference
between the sample pool and standards (P > 0.05). The
accuracy of the procedure was (125.27 6 3.18)%. To
assess procedural variance we ran two pools and for the
ﬁrst the inter/intra-assay coefﬁcient of variance was
19.8/5.1, while for the second it was 21.3/5.
Assessment of changes in food availability
To assess the changes in the food available in each of
the fragments, we identiﬁed and measured diameter at
breast height (DBH) of all trees greater than 10 cm
DBH in 2000 and again in 2003. When trees were on
extremely steep sides of the craters, their size was visually estimated (error in visual estimation ¼ 63.8%). As
colobus monkeys rarely feed in small trees (Gillespie and
Chapman, 2001), this represents a nearly complete inventory of all major potential colobus food sources. Subsequently, trees were classiﬁed as important food trees if
they were in the top ﬁve most frequently eaten species
at any of the seven sites within Kibale forest or at one
forest fragment. This is based on 3,355 h of observations
(Chapman et al., 2002b). A number of studies support
the use of DBH or basal area as an indicator of plant
productivity (Catchpole and Wheeler, 1992; Chapman
et al., 1992).
Analysis
Our overall objective was to determine if changes in
the abundance of red colobus or population stress level
(cortisol and variance in cortisol) in the fragments were
related to changes in food availability or parasite infections. To meet this objective we index change in food
availability by the change in the cumulative DBH of food
trees available to the populations between 2000 and
2003 expressed as change in cm DBH/ha. However, to
examine associations with parasite infections is not so
straight forward, since there are a number of indices
available to describe the infections. Thus, we ﬁrst present correlations between population differences, cortisol
level, variance in cortisol level, and descriptors of parasite infections. Subsequently, we conduct stepwise multiple regressions to determine which combination of the
major descriptors of parasite infection best predicted the
dependent variables. Since the number of fragments is
small (n ¼ 8) and since some authors have pointed out
problems with stepwise multiple regressions (James and
McCulloch, 1990; Bronikowski and Altmann, 1996), we
also used the two independent variables with the highest
Pearson correlation coefﬁcients in a forced entry regression to predict the dependent variables. These regressions mirrored the results of the stepwise multiple
regressions in indicating the most important predictor
variable and thus are not reported. Since we had a priori
predictions of how population change and cortisol would
respond to changes in food availability and parasite
infections, one-tailed tests are reported. Next, because
many of the potential explanatory factors (i.e., indices of
parasite infections) were auto-correlated, path analysis
were used to determine the potential structuring of the
relationships among variables.
For our purposes, path analysis is very useful since
the path coefﬁcients among the variables allow the
determination of the magnitude of both direct and indirect effects among variables. In our study, we are particularly interested in the indirect effects of how changes
in food supply inﬂuence population change through its
impact on susceptibility to parasite infection. Path analysis begins with the construction of a path diagram
showing the relationships among the variables in the
system based on a priori knowledge of how the system
operates (Kingsolver and Schemske, 1991). In our case
this means that the diagram is based or rooted on
changes in food availability, which can have a direct
effect on population size, or an indirect effect on population size via parasite infections. In these analyses there
are a number of independent variables measured with
different units, but the path coefﬁcients, or beta coefﬁcients, are standardized regression coefﬁcients that allow
one to compare the relative effect on the dependent
variable of each independent variable. Despite the advantages of path analysis, it should not be used to infer
causation among variables (Shipley, 1999). Rather path
analysis identiﬁes correlations among variables, including both direct and indirect effects, and these represent
possible targets of selections that can be further tested
using an experimental approach (Kingsolver and Schemske,
1991). Since the number of fragments that still maintained large sizable colobus at the end of the study was
few, and since there are many indices of parasite infections, in both the path analysis and the stepwise multiple regression, we considered only major indices of parasite infections (richness, prevalence of all nematodes,
American Journal of Physical Anthropology—DOI 10.1002/ajpa
529
FOOD AVAILABILITY, PARASITISM, AND STRESS
TABLE 1. Descriptions of the density, tree community, cortisol, and gastrointestinal infections of the red colobus
(Piliocolobus tephrosceles) in a series of forest fragments neighboring Kibale National Park, Uganda
Fragment
CK Durama
Kiko II
Kiko III
Kiko IV
Kiko1
Lake
Nyaherya
Lake
Nkuruba
Rutoma
Fragment type
Number of households
Activity in the fragment
Density 2003 (ind/ha)
% Change in density
Trees/hectare 2003
% Change in food DBH
Stumps/hectare
Cortisol (ng/g)
Richness
Prevalence of Nematode
Prevalence of Trichuris
Prevalence of
Strongyloides fullebornii
Prevalence of
Strongyloides stercalis
Prevalence of
Oesophagostomum
Prevalence of
strongyle nematode
Trichuris egg/g
All Nematodes egg/g
Proportion with
Multiple Infections
Valley þ Hill
16
B, G, L, W
2.30
25.00
86
14.24
45.75
139.23
0.49
47.46
45.76
0
Valley
6
C, W
2.6
18.75
63
58.91
8.40
386.68
0.88
78.05
63.41
7.32
Valley
3
W
8.24
41.67
171
41.43
221.76
445.12
1.29
83.33
54.17
16.67
Valley
5
W
11.67
41.67
230
24.08
174.17
230.66
0.667
66.67
60.00
3.33
Valley
9
L, W
2.10
27.78
38
71.92
56.45
165.68
0.91
73.17
62.79
11.63
Crater lake
8
C, L, W
0.65
57.14
30
12.18
15.00
144.10
0.44
44.44
33.33
0
Crater lake
2
W
3.28
16.67
40
2.89
1.00
245.85
0.294
29.41
27.54
0
Hill side
8
G, W
7.50
25.00
28
16.21
337.50
356.03
0.4
38.18
36.36
0
0
0
12.5
0
0
0
1.69
7.32
16.67
3.33
4.65
1.69
4.88
16.67
0.00
11.63
2.02
2.05
1.69
9.2
9.65
9.76
3.8
9.68
33.33
2.5
8.42
0
8.84
2.57
23.26
0
0
0.27
0.00
0
0
3.64
0.44
1.36
0
1.4
0.56
0
3.3
3.36
1.82
11.11
For Activity type, B, beer; G, gin; C, charcoal; L, livestock, and W, woodlot.
egg/g of all nematodes) and did not consider individual
parasite indices (e.g., prevalence of Oesophagostomum
sp.). We also limit our path analyses to simple models
involving three variables and report both signiﬁcant and
nonsigniﬁcant path coefﬁcients, recognizing that a comparison of the size of the coefﬁcient is indicative of the
size of an effect among variables.
RESULTS
Red colobus population change
in forest fragments
Of the original 19 fragments surveyed in 1995, 11 supported red colobus in 2000 and nine in 2003. None of the
original fragments occupied by red colobus were cleared in
the 8 years between censuses. In 2000 we counted 127 red
colobus in the eight fragments we considered, while in
2003, 102 animals were seen in those same fragments. In
the 2000 census, 55 adult female red colobus were counted
and the ratio of infants to adult females was 0.31. In the
2003 census, 54 adult females were counted and the ratio
of infants to adult females was 0.19. The age/sex class
that declined the most was the subadult category and
there were 4 times fewer subadults in 2003 than there
were in 2000. Among the eight fragments monitored in
2000 and 2003, populations declined at an average of 22%;
however, population change over this period was highly
variable and ranged from an increase of 25% to a decline
of 57%. The change in red colobus density (mean change
¼ 0.71 individuals/hectare, density range ¼ 8.3–9.2 individuals/hectare, n ¼ 8 fragments) was not correlated to
the either size of the fragment, the number of households
using it, or its distance to either Kibale or the nearest
fragment (P > 0.272 in all cases, n ¼ 8).
Changes in forest attributes
In all fragments we found evidence of forest clearing;
however, the extent of clearing was extremely variable.
The average size of the fragments containing red colobus
was 4.4 hectare (n ¼ 8 measured in 2000). In 2000 there
were on average 99 trees/hectare (range 27–259 trees/hectare), while in 2003 there were 86 trees/hectare (range
30–230 trees/hectare). The basal area of trees in the fragments averaged 9002 m2 in 2000 (range 1,981–39,012 m2)
and 5,293 m2 (range 1,772–28,397 m2) in 2003, and the
cumulative basal area of food trees was 915 m2 in 2000
(range 317–2,430 m2) and 535 m2 (42–2,387 m2) in 2003.
Thus, on average the basal area of food trees declined by
29.5% over the 3 years; however, forest change was highly
variable. Lake Nkuruba, the site of a community-based
conservation project, exhibited a 2% gain in food tree basal area, which is comparable to rates of growth of trees
in undisturbed forest in the region (Chapman and Chapman, 2004). In contrast, forest clearing led to a 71%
decline in food tree basal area in a fragment within a tea
plantation. In 2000, exotic species, primarily Eucalyptus
sp. constituted 16% of the food tree basal area, while in
2003 this value had risen to 28%. There was little change
in tree richness between time periods (2000 ¼ 11.5 species/hectare, 2003 ¼ 11.6 species/hectare).
Parasite community
The parasite communities described from the 634 red
colobus fecal samples collected from the eight forest fragments between August 1999 and June 2004 included the
following nematodes: Trichuris sp. (Superfamily Trichuroidea), Oesophagostomum sp. (Superfamily Strongyloidea),
Strongyloides fuelleborni, S. stercoralis (Superfamily Rhabditoidea), and an unidentiﬁed strongyle. We also identiﬁed
three protozoans, Entamoeba coli, E. histolytica/dispar,
American Journal of Physical Anthropology—DOI 10.1002/ajpa
530
C.A. CHAPMAN ET AL.
Fig. 1. The cortisol levels
(6SE) measured from red colobus monkeys (Piliocolobus tephrosceles) in a series of forest
fragments neighboring Kibale
National Park, Uganda and the
corresponding population change
in that fragment.
and Giardia sp. (likely G. lamblia). Additionally, in one
individual, an Ascaris sp. egg (Superfamily Ascaroidea) was
found. However, because of the difﬁculty of quantifying protozoan infections and the small sample size for the Ascaris
sp., these parasites are not considered further.
On average, three of the ﬁve major parasite species were
found in any one fragment, but this ranged from 1 to 5 species. The number of species found was independent of the
number of samples collected (Spearman rank correlation
rsp ¼ 0.160, P ¼ 0.706). The average parasite richness of
all individuals averaged 0.67 species (range 0.40–1.29 species), while the richness in infected individuals averaged
1.14 (range 1–1.55; Table 1). The percentage of the population in each fragment that had multiple infections average
8.7% (range 0–33%). Nematode prevalence averaged 58%
across the fragments (range 29–83%). This was strongly
inﬂuenced by the abundance of Trichuris sp., which had an
average prevalence of 48% (range 28–63%). Mean prevalence of Oesophagostomum sp. was 5.6% (range 0–17%). S.
fulleborni prevalence averaged 4.9% (range 0–17%). The
prevalence of S. stercoralis was the lowest of all nematodes
examined, averaging 1.6% (range 0–13%). Mean prevalence
of the unidentiﬁed strongyle was 4.8% (range 0–17%). The
average number of parasite egg/g averaged 4.71 among
fragments (range 0.56–9.68 eggs/g). These values were
heavily inﬂuenced by the abundance of Trichuris sp., which
on average had 3.94 eggs/g among fragments (0.44–8.84
egg/g; Table 1).
Gillespie and Chapman (2006) have previously documented elevated parasite infections in primate in forest
fragments compared to groups in the main forest. Analyzing the smaller subset of fragments here documents similar differences to those reported earlier (e.g., nematode
prevalence: forest in Kibale National Park ¼ 41.73, in
fragments 57.59; Trichuris sp. prevalence 40.77, 47.92,
Oesophagostomum prevalence 0.96, 5.63, nematode egg/g
2.51, 4.71; proportion of multiple infections 3.54, 8.73).
Cortisol levels
Cortisol levels averaged 264 ng/g among fragments,
but ranged from 140 to 446 ng/g. The cortisol levels for
the fragments were not correlated with the number of
samples collected (r ¼ 0.160, P ¼ 0.704). The fragment
with the least cortisol in the samples was 2.7 times less
than the fragment with the highest cortisol level (see
Fig. 1). Further, the fragment with the most variable
cortisol levels was 4.3 times more variable than the least
variable fragment. The estimate of the variance in cortisol level within a population was not related to the number of samples analyzed for that population (r ¼ 0.286,
P ¼ 0.197).
The cortisol levels for groups in the intact forest of
Kibale National Park were *3.5 times lower than the
average value for the forest fragments when comparisons
are made to the same month of collection or the same
month in the subsequent year (Kibale Group 1 June 2003
¼ 76.4 ng/g, range 44.6–154.4 ng/g; Group 1 June 2004 ¼
82.9 ng/g, range 42.9–153.2 ng/g; Group 2 June 2004 ¼
66.3 ng/g, range 31.0 to 145.4 ng/g). Animals from the continuous forest seldom had values as high as the lowest
value from the fragments.
Population change and stress in relation
to food availability and parasitism
An increased rate of forest loss (i.e., decline in cumulative DBH of food trees) was related to a decrease in population size (Table 2), but it also was associated with an
increase in indices of parasitic infection, and an increase
in parasitism also corresponded to a decline in population size. With respect to cortisol, the picture is not as
clear. An increase in deforestation was only marginally
related to elevated cortisol levels (P ¼ 0.055; Table 2).
However, an increase in cortisol was related to an
increase in some of the indices of parasite infections.
There was no signiﬁcant correlation between population
change and cortisol levels.
In stepwise multiple regressions predicting population
change or variance in cortisol, only changes in food
availability entered the stepwise regression (population
change r2 ¼ 0.685, P ¼ 0.011; variance in cortisol r2
¼ 0.664, P ¼ 0.014). When attempting to predict cortisol
American Journal of Physical Anthropology—DOI 10.1002/ajpa
531
FOOD AVAILABILITY, PARASITISM, AND STRESS
TABLE 2. Correlations between population change, fecal cortisol level, variance in fecal cortisol, and food availability
in red colobus in a series of forest fragments neighboring Kibale National Park, Uganda
Population change
Predictor
Cortisol
Variance in cortisol
r
P
r
P
r
P
Major variable
Change in food availability
Parasite richness
Prevalence of nematodes
Nematode egg/g
Proportion of multiple infections
0.827
0.668
0.689
0.692
0.505
0.006
0.035
0.029
0.029
0.101
0.599
0.530
0.414
0.713
0.464
0.055
0.088
0.154
0.024
0.123
0.801
0.634
0.498
0.649
0.626
0.008
0.046
0.105
0.048
0.048
Minor variable
Prevalence Trichuris sp.
Prevalence Oesophagostomumsp.
Prevalence Strongyloides fuelleborni
Prevalence S. stercoralis
Prevalence unidentiﬁed strongyle
Egg/g Trichuris sp.
0.548
0.593
0.621
0.510
0.488
0.201
0.080
0.061
0.050
0.099
0.110
0.317
0.212
0.373
0.500
0.621
0.509
0.305
0.308
0.180
0.103
0.050
0.099
0.231
0.307
0.412
0.629
0.669
0.699
0.365
0.230
0.155
0.047
0.035
0.027
0.187
Pearson correlation coefﬁcient and probability levels, with signiﬁcant values in italic. Egg/g is only presented for Trichuris sp. since
for the other species it was rare to ﬁnd more than 1 egg per sample.
TABLE 3. Path coefﬁcients of changes in food availability and
indices of parasitism on changes in red colobus population size,
cortisol level, and variance in cortisol level in the red colobus
(Piliocolobus tephrosceles) populations inhabiting a series of
forest fragments adjacent to Kibale National Park, Uganda
Population Change
1st model
Richness
Food availability
0.609
Richness
–
Pop change
0.668
0.262
Indirect path
0.159
2nd model
Prevalence Pop change
Food availability
0.575
0.644
Prevalence
–
0.319
Indirect path
0.183
3rd model
Egg/g
Food availability
0.710
Egg/g
–
Pop change
0.677
0.211
Indirect path
0.150
Cortisol
1st model
Richness
Food availability
0.537
Richness
–
Cortisol
0.433
0.281
Indirect path
0.149
2nd model
Prevalence Cortisol
Food availability
0.537
0.499
Prevalence
–
0.133
Indirect path
0.071
3rd model
Egg/g
Food availability
0.685
Egg/g
–
Cortisol
0.230
0.513
Indirect path
0.352
Variance in Cortisol
1st Model
Richness
Food availability
0.573
Richness
–
Variance in cortisol Indirect path
0.690
0.203
0.219
2nd model
Prevalence Variance in cortisol Indirect path
Food availability
0.537
0.729
0.078
Prevalence
–
0.135
3rd model
Egg/g
Food availability
0.685
Egg/g
–
Variance in cortisol Indirect path
0.642
0.126
0.230
Pathways for the parasite indices are presented in Figure 1.
Signiﬁcant coefﬁcients are in italic.
level, only the egg/g of all nematodes entered the equation (r2 ¼ 0.507, P ¼ 0.0487).
We produced simple path analyses that considered each
major index of parasite infection separately along with
food availability (indexed as the loss in food trees (cm
DBH/ha)) to predict population change (Table 3, Fig. 2).
Fig. 2. An example, path analysis of factors predicted to
affect the change in population size of red colobus monkeys
(Piliocolobus tephrosceles) in a series of forest fragments neighboring Kibale National Park, Uganda. Positive effects are indicated by solid lines and negative effects by dashed lines. Double
headed arrows indicate positive relationships between predictor
variables. The width of the arrow indicates the magnitude of
the standardized path coefﬁcients. Signiﬁcant pathways and
path coefﬁcients are shown in Table 2, which also presents the
same information with other predictors of population change,
cortisol, and variance in cortisol.
Each of these analyses indicated that reduced food availability had a direct effect on population size leading to
decline (Table 3) and in all cases the path coefﬁcient was
relatively large (mean ¼ 0.663). Reduced food availability
also had an indirect effect on population size through its
inﬂuence on parasite infections. Here reduced food availability had an initial fairly strong effect on the indices of
parasitism considered (mean ¼ 0.631), which subsequently
had weaker and negative effects on population size (mean
¼ 0.264). As an example, while the direct effect of
changes in food availability on population change is relatively large (0.677), as is the indirect effect of changes in
food availability on nematode eggs/g (0.710), the effect of
changes in nematode eggs/g on population change is rela-
American Journal of Physical Anthropology—DOI 10.1002/ajpa
532
C.A. CHAPMAN ET AL.
tively small (mean ¼ 0.211). Thus, the total indirect
effects are relatively small (0.710 3 0.210 ¼ 0.15;
Fig. 2) compared to the direct effect (0.677).
Including cortisol or the variance in cortisol in such
three variable path analyses similarly suggests that
reduced food availability has a large direct effect, but a
small indirect effect, with one exception. In a three variable path (food availability, nematode load, and cortisol),
the indirect path involving food availability and nematode load was stronger (path coefﬁcient ¼ 0.352) than
the direct path (path coefﬁcient ¼ 0.230).
DISCUSSION
We found support for our prediction that there would
be positive associations between population change, loss
of food resources, and parasitic infections. Red colobus
abundance declined with the loss of food trees, indicating
that the availability of food resources is a major determinant of colobus population size. This ﬁnding is counter
to the claim that folivore food resources are superabundant and evenly dispersed, and thus within-group
scramble competition is weak or absent among folivorous
primates (Wrangham, 1980; Isbell, 1991).
Population declines were also negatively associated
with a number of the indices of parasite infection. This
may reﬂect the direct negative inﬂuence of these gastrointestinal parasites, or, as is suggested by the path analysis that these parasites are taking advantage of a
decline in the animal’s immune system that is associated
with poor nutrition. Several of the parasites infecting
colobus in the Kibale region have the capacity to cause
substantial pathology at high prevalence. Heavy infections of Oesophogostomum sp. and Strongyloides sp. are
associated with mucosal inﬂammation, ulceration, dysentery, weight loss, and death. Even moderate infections of
Oesophogostomum sp. have proven clinically important
in stressed captive primates (Crestian and Crespeau,
1975). However, other parasites, like Trichuris sp., are
typically asymptomatic and may not affect demography.
Despite the potential of some parasites to cause pathology, the path analysis suggests that the direct effect of
loss of food resources is *4 times greater than the indirect effects of increased parasitism. It is possible that
the effect of parasites might have been stronger, since by
sampling throughout the period we could be sampling
those animals left in fragments that are most ﬁt and are
able to survive under the parasite and nutrient conditions of the fragmented forest. Evidence from one fragment monitored over 5 years following a marked change
in density suggests that as populations decline parasite
infections remain high. Following the clearing of a forest
fragment supporting red colobus and black-and-white
colobus (Colobus guereza), animals moved into a neighboring fragment that we had been monitoring for a number of years and for which we were routinely monitoring
parasite infections (Chapman et al., 2005). The immigration of animals into the fragment resulted in the colobus
populations more than doubling and colobus density
becoming almost twice that found in Kibale. In both colobus species the prevalence of Trichuris sp. increased.
Over the next 5 years the prevalence and intensity of
infection of Trichuris sp. in red colobus declined and
their population numbers slowly increased. In contrast,
the prevalence and intensity of infection of Trichuris sp.
increased in black-and-white colobus and remained high
following the immigration and their population size
declined. The challenge of applying this information to
conservation is to connect the patterns we have documented to the reproductive success of individuals that
vary in their severity of parasite infection (i.e., quantifying a change in parasitism with a change in ﬁtness). An
experimental approach that reduces parasite infections
would be most revealing.
Cortisol was not related to population change, but the
number of nematode egg/g found in their feces was positively associated with cortisol, and it was marginally
related to other indices of parasite infections. There are
a number of plausible explanations for the lack of association between cortisol level and population change. We
used methodologies that would minimize variance that
was unrelated to ecological factors (e.g., time of the day,
age, reproductive condition); however, we could not control for social factors that could stress animals. Future
studies should consider partitioning the variance in cortisol levels between ecological and social stressors. Interestingly, there was a weak association between the variance in a population’s cortisol level and population
change, with populations with more variable cortisol levels declining the most. Furthermore, the variance in cortisol was related to a number of indices of parasite infections. These ﬁndings highlight the importance of examining cortisol levels at an individual level, as well as at
the population level, to understand how it varies with
social factors and if these social factors are inﬂuenced by
changes in ecological conditions. For example, dominant
individuals may have improved access to resources that
could boost overall condition and immunocompetence, or
high rank may lead to increased need to assert dominance in ecologically stressful times, more ﬁghts, and
higher levels of stress (Combes, 2001; Abbott et al.,
2003). The lack of association between cortisol level and
population decline may also reﬂect that some of our
measurements were from populations that were only
experiencing stress on the short term (e.g., short-term
food shortage), while cortisol would have to be chronically elevated to high proportions to be responsible for a
decline in population size. Thus, evaluation of cortisol
levels in these populations over an annual cycle may
illustrate a stronger association between stress and population change. Furthermore, there is the need to critically evaluate methods of evaluating cortisol to address
conservation questions such as the one being addressed
here. Some animals naturally have higher cortisol levels
than others (Muehlenbein, in press), and cortisol can
vary along a number of dimensions (e.g., positive as well
as negative emotions; (Pollard, 1995), group size (Pride,
2005)). Thus, at this time it is premature to make an
evaluation of the use of cortisol to address such conservation issues and it is clear that the academic community needs to evaluate sources of variation in cortisol levels so that these can be controlled for in further applications of this tool.
Our ﬁndings support suggestions that nutritional status interacts with the host immune response and leads
to a synergistic relationship between food availability
and parasites to inﬂuence population change (Gulland,
1992; Holmes, 1995; Murray et al., 1998), but suggest
that the direct effect of food availability has the strongest inﬂuence. Previous research examining population
cycles has suggested the potential for such synergy at
periods of peak density in the cycle, since at these times
animals often face food shortages (Keymer and Dobson,
1987; Murray et al., 1996, 1998). But it also seems possi-
American Journal of Physical Anthropology—DOI 10.1002/ajpa
FOOD AVAILABILITY, PARASITISM, AND STRESS
ble that this synergy operates in non-cycling species and
not necessarily during periods of peak density, but when
density is high relative to food availability. The situation
we examined was an artiﬁcial one created by human habitat modiﬁcations where food resources were removed rapidly. Thus, the importance of the interaction of nutritional
status and parasitism on population size in more natural
systems needs to be examined. However, based on our
past studies of variability in food availability for folivores
(temporal and spatial; (Chapman et al., 2004b), along with
the ﬁndings here in forest fragments where reduced food
availability had the strongest inﬂuence on population
change, it is likely that this synergistic relationship is critical in the population dynamics of red colobus in both
human modiﬁed and unmodiﬁed habitats.
Understanding the ecological determinants of animal
abundance has been a central question in the ﬁeld of
ecology since its inception. However, this issue has taken
on new importance given the current rate of anthropogenic disturbance, the subsequent decline in many wildlife species, and the need to construct informed management plans. With respect to primates, these theoretical
issues are critical because the tropical forests they
occupy are undergoing rapid anthropogenic transformation. Cumulatively, countries with primate populations
are losing *125,000 km2 of forest annually (Chapman
and Peres, 2001). Other populations are affected by forest degradation (logging and ﬁre) and hunting. Based on
patterns of rural development and land conversion, we
expected a decline in population size of red colobus living
in unprotected fragments and this expectation was borne
out by the surveys. These ﬁndings suggest a low conservation value for small unprotected forest fragments that
provide communal resources. It is likely that most of
these fragments will be destroyed and the colobus populations they support lost within this decade. However,
the rate of conversion is highly variable depending on
the needs of local land owners. It was this pattern of
variability that allowed us to examine the interactive
effects of food availability and parasitism on red colobus
abundance. Examining this variability suggested that
the loss of food trees associated with people using forests
strongly affects colobus and leads to population declines.
However, forest conversion also appeared to affect the
colobus populations through its effect on parasitic infections. Since we have previously demonstrated that
human modiﬁcations to landscapes can alter interactions
between parasites and hosts (i.e., selective logging; (Gillespie et al., 2005a), this raises the intriguing question
of what types of anthropogenic disturbances will lead to
disease playing a more signiﬁcant role in determining
primate population size. In the future, between-site comparisons should be chosen carefully to explore the modifying effects of speciﬁc anthropogenic disturbances (e.g.,
forest fragmentation with or without elevated rates of
human contact); because the focus has now shifted from
whether anthropogenic habitat change alters primatedisease interactions to how anthropogenic change alters
primate-disease interactions.
CONCLUSIONS
Identifying factors that inﬂuence primate density is
critical in the development of informed conservation
plans; however, there are few general models explaining
variation in abundance. Here we studied a series of forest fragments outside of Kibale National Park, Uganda
533
to examine if food availability and parasite infections
could have synergistic affects on red colobus (Piliocolobus tephrosceles) abundance. Given that primate population size can respond very slowly to even dramatic environmental change, we also quantiﬁed fecal cortisol levels. Evidence suggests that a decline in food availability
has a direct and negative effect on colobus population
size, as well as an indirect effect of parasite infections,
which in turn negatively impacts colobus abundance.
The use of cortisol to monitor population status was ambiguous as it was only marginally related to declines in
food availability, related to only some indices of parasite
infections and not related to population change. Thus, at
this time it is premature to make an evaluation of the
use of cortisol to address such conservation issues using
the approaches applied here.
ACKNOWLEDGMENTS
Permission to conduct this research was given by the
National Council for Science and Technology, and the
Uganda Wildlife Authority. L. Chapman, E. Greiner, and
M. Huffman provided helpful comments on this research
and E. Greiner aided in parasite identiﬁcation.
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American Journal of Physical Anthropology—DOI 10.1002/ajpa